The abundance, biomass and composition of pelagic ciliates in East African lakes of
different salinity and trophy
A. W. Yasindi1,2 and W. D. Taylor1
1
2
Department of Biology, University of Waterloo, Ontario N2L 3G1, Canada.
Corresponding author, present address: Department of Zoology, Egerton University, P. O. Box 536, Njoro,
Kenya
E-mail: [email protected], [email protected]
Abstract
Planktonic ciliates were studied in 17 tropical East African
lakes of different salinity and trophic status. Oligotrichs
(e.g., Strombidium, Strobilidium and Halteria) and
scuticociliates (e.g., Cyclidium, Pleuronema, Cristigera),
dominated the ciliate communities. Conductivity and
trophic status were the most important environmental
variables influencing the distribution of ciliate species in
East African lakes. Herbivorous oligotrichs were important
in oligotrophic and mesotrophic lakes, as they are in
temperate and subtropical lakes, but their importance
decreased with increasing chlorophyll a concentration and
conductivity. On the other hand, the importance of
scuticociliates (primarily bacterivores) increased with
increasing chlorophyll a and conductivity.
Mean ciliate abundance ranged from 2 to 1,220
ciliates.mL-1 while the biomass range was from 1.9 to 1,
900 µg C.L-1 respectively from oligotrophic to eutrophic
lakes. Abundance and biomass had positive relationships
with phytoplankton biomass. The ciliate abundance and
biomass were higher than those reported in temperate
(Quebec) and subtropical (Florida) lakes of similar trophic
status. However, regression models predicting abundance
and biomass of ciliates from chlorophyll suggest that
temperate (Quebec), subtropical (Florida) and tropical
(East Africa) lakes have similar ciliate abundance and
biomass per unit chlorophyll except some saline tropical
lakes which have very high abundance and biomass of
ciliates relative to chlorophyll.
Key words: Ciliated protozoa, high abundance and
biomass, tropical lakes.
Introduction
Ciliates comprise a significant component of the
abundance and biomass of freshwater plankton
communities. Their densities may be between 1-30
ciliates/ml in oligotrophic and mesotrophic lakes but
may be exceed 1000/ml in eutrophic lakes (Yasindi
et al. 2002). Ciliates feed on bacteria, pico- and
nanophytoplankton but they are prey for zooplankton
and fish larvae (Porter et al. 1979). As such, ciliates
form a link in the process of energy flow from the
smallest plankton groups to the higher trophic levels.
Some studies have found a significant relationship
between the abundance and biomass of planktonic
ciliates and lake trophic state as measured by
chlorophyll a concentration (Beaver and Crisman,
1982). Ciliate species diversity and richness are also
influenced by lake productivity whereby the most
productive lakes have the highest diversity and
richness. The type of food items also influences the
distribution of ciliate species. Large oligotrichs (>30
µm), which graze on nanophytoplankton, dominate
oligotrophic lakes while small ciliates (<30 µm) that
graze on bacteria dominate eutrophic lakes in
temperate and subtropical lakes (Beaver and
Crisman, 1982). However, most studies of
planktonic ciliates have mainly been confined to the
temperate lakes with relatively few studies in
subtropical and tropical waters. Previous studies of
ciliates in tropical freshwater lakes have been
confined to single lakes (Finlay et al. 1987; Taylor &
Zinabu 1989; Yasindi 1995). Therefore, our
knowledge of planktonic ciliates of tropical
freshwaters in general and East African lakes in
particular is still very poor. The goal of this study
was to investigate the abundance, biomass,
composition and the ecological role of ciliates in the
food webs of tropical East African lakes of different
salinity and trophic status and compare with
previous studies intemperate lakes.
Materials and methods
Ciliate samples were taken from 17 lakes including
Lakes Awassa, Abijata, Chamo, Langano and Zwai
in Ethiopia and Lakes Baringo, Bogoria, Solai,
Nakuru, Elmenteita, Naivasha, Oloidien, Sonachi,
Simbi, Victoria, Malawi and Crescent lake in Kenya.
250-mL ciliate samples were collected in triplicate
using a 4-L Van Dorn sampler at different depths,
and immediately fixed in concentrated Bouin’s fluid
(5% v/v final concentration). In the laboratory, the
water samples were concentrated to 50 ml by
settling for 48 h. Subsamples of 0.5 to 5 mL (from
eutrophic to oligotrophic lakes) were filtered onto
gridded filters and stained by Quantitative Protargol
Staining (QPS) technique of Montagnes & Lynn
(1993). Ciliates were identified to genus or species
level and enumerated. To determine ciliate biomass,
ciliate dimensions were measured on a
Summasketch III digitizing tablet and using
microbiota software, which equates ciliates to
standard geometric shapes such as cones, sphere
and prolate spheroids (Roff & Hopcroft, 1986). The
biovolume was then converted to biomass using a
volume to carbon ratio of 0.14 pg C. µm-3 (Putt &
Stoecker, 1989). Ciliates were counted either by
scanning the whole stained filter when ciliate density
was low or by counting ciliates in three randomly
selected squares until 100 to 200 ciliates were
counted. Species diversity was calculated based on
Shannon diversity index using the MVSP (Kovac
1999). Ciliate size was expressed as equivalent
spherical diameter (ESD) using the formula: ESD =
0.4775 Vol 1/3. Chlorophyll a concentration was
374
measured and used as an indicator of trophic status.
Bacteria were counted using the acridine-orange
direct-count method of Hobbie et al. (1977).
Physico-chemical factors such astemperature, pH,
DO, alkalinity, conductivity and transparency were
also measured.
We used the classification of lakes based on their
ranges of conductivity by Talling & Talling (1965) to
assign the lakes with conductivity < 600 µS.cm-1 to
freshwater lakes, lakes with conductivity between
600 - 6000 µS.cm-1 as moderately saline lakes and
saline lakes as lakes with conductivity > 6,000
µS.cm-1.
According to chlorophyll range group 1 (or
oligotrophic) comprised Malawi (< 5 mg.m-3), group
2 (mesotrophic) had Naivasha, Oloidien, Victoria,
Solai, Nakuru, Elmenteita, Sonachi, Simbi, and
Bogoria (5-50 mg.m-3), and Baringo, Abijata, Chamo,
Awassa, Zwai, and Langano (> 50 mg.m-3) formed
Group 3 (eutrophic). We used the classification of
lakes based on conductivityby Talling and Talling
(1965) to assign the lakes with conductivity range of
207 - 350 µS·cm-1 to freshwater lakes (< 600 µS·.cm1
), lakes with 850 - 5,457 µS·cm-1 as moderately
saline lakes (600 – 6,000 µS·.cm-1) and lakes
between 11,824.5 –16,837 µS·cm-1 as saline (>
6,000 µS·cm-1) lakes.
Bivariate regression and multiple regression
(Statsoft, Inc. 1995) were used to assess
relationships between ciliate abundance and
biomass with environmental factors.
Table 1. Abundance, biomass and environmental variables measured. Abun = Abundance, Biom = biomass,
Cond = conductivity, Temp = temperature, DO = dissolved oxygen, Alk = alkalinity, Chl a = Chlorophyll a and
Bact = bacteria.
Lake
Abun
Biom
Cond
pH
Temp
DO
Alk
Chl a
Bact
Secchi
n
Baringo
5.6 ± 0.7
22 ± 19.6
912.0
8.2
25.2
9.3
233.3
43 ± 12
9.1
0.61
18
Bogoria
43.5 ± 8.2
220 ± 150
69792.0
9.4
26.9
12.9
14316.7
266 ± 8.9
66.7
0.13
6
Solai
21.7 ± 19
25 ± 22
5457.0
8.6
26.0
6.4
885.7
209 ± 11
42.9
0.07
6
Nakuru
32.4± 40.7
31± 68
16837.0
9.4
24.7
17.8
70.4
123 ±0.5
255.9
0.12
3
Elmenteita
640.3 ± 578
971 ± 763
15807.9
9.7
20.9
8.5
1973.6
123 ± 9.2
245.0
0.15
33
Sonachi
377.9 ± 70
1900 ± 1344
11824.5
9.5
21.3
8.8
1855.4
89 ± 6.9
40.5
0.16
63
Crescent
3.6 ±2.6
17 ± 11
294.4.0
7.7
20.0
3.9
24.6
32 ± 15
9.5
1.22
15
Naivasha
3.4 ± 0.4
17 ± 7
319.4
7.8
19.9
6.4
49.9
26 ± 1.9
8.2
1.07
75
Oloidien
6.9 ± 1.2
30 ± 12.6
2466.7
9.3
21.4
-
312.0
23.0
97.2
0.25
15
Simbi
2.9 ± 1.2
12 ± 8.5
21241.0
9.3
25.5
4.9
1860.1
82 ± 3
35.7
0.93
15
Victoria
12 ± 4.3
43 ± 13.2
207.0
6.4
26.2
6.7
-
31 ± 2.3
8.3
0.92
45
Malawi
2.2 ± 0.7
2.3 ± 0.7
256.1
-
24.9
7.3
-
1.5
2.9
20.00
66
Zwai
8.8 ± 0..2
42 ± 9
350 ± 5.8
8.5 ± 0.2
18 ± 0.1
-
4 ± 0.4
27.3
11.3
0.30
6
Langano
3.1 ± 0.9
22.7 ± 11
1580 ± 200
9.5 ± 0.1
24 ± 0.6
-
14 ± 0.4
13.4
7.0
0.23
12
Chamo
5.3 ± 44.7
11 ± 2.2
1320
8.9
-
-
12
44.2
16.7
0.65
3
Abijata
15.2 ± 13.8
60 ± 10.5
21500 ± 866
10 ± 0.1
24 ± 0.5
-
250 ± 32
11.6
43.8
0.65
3
Awassa
8.1 ± 1.9
8.9 ± 2.2
850 ± 288
8.3 ± 0.2
21 ± 0.4
-
9 ± 1.4
11.8
9.5
1.38
15
375
0.8
0.5
Zwai
Victoria
III
Awassa
Langano 0.3
Chamo
Bar
Solai
A x is 2
Oloidien
-1.4
-1.1
-0.8
-0.5
-0.3
Abijata
0.3
Simbi
Nakuru
Sonachi
0.5 Elm
0.8
Bogoria
-0.3
Malawi
-0.5
-0.8
-1.1
-1.4
Axis 1
Figure 1. Principal components analysis diagram based on 6 environmental variables showing the
distribution of the East African lakes on the first two principal components. The first axis is horizontal and the
second is vertical. Bar = Baringo, Elm = Elmenteita, I = Crescent, II = Naivasha.
Table 2. The correlation matrix for ciliate biomass and environmental variables. Log10-transformed means of
all data for two years combined were used. Abbreviations as in Table 1. * = r is significant at 0.05 level of
significance.
1
2
Biomass Temp pH
Biomass 1.00
Temp
0.18
PH
0.53*
Cond
0.59*
Alk
0.39
Do
0.62*
Bact
0.74*
Chl a
0.65*
Secchi -0.68*
0.18
1.00
-0.13
0.24
0.41
0.43
0.11
0.07
-0.07
Cond Alk
DO
Bact Chl a Secchi
0.53* 0.59* 0.39 0.62* 0.74* 0.65* -0.68*
-0.13 0.24 0.41 0.43 0.11 0.07 -0.07
1.00 0.61* 0.56* -0.06 0.62* 0.63* -0.79*
0.61* 1.00 0.79* 0.40 0.81* 0.64* -0.59*
0.56* 0.79* 1.00 0.33 0.69* 0.63* -0.59*
-0.06 0.40 0.33 1.00 0.43 0.56* -0.26
0.62* 0.81* 0.69* 0.43 1.00 0.75* -0.71*
0.63* 0.64* 0.63* 0.56* 0.75* 1.00 -0.82*
-0.79* -0.59* -0.59* -0.26 -0.71* -0.82* 1.00
Results
Principal
Component
Analysis
(PCA)
of
environmental variables divided the lakes into
oligotrophic, mesotrophic and eutrophic lakes
(Figure 1). 49 ciliate genera were identified from the
17 lakes. Small ciliates (< 30 µm ESD), mainly
Strobilidium,
Strombidium,
and
Halteria
(Oligotrichida), and Cyclidiun, Cristigera, and
Pleuronema
(Scuticociliatida)
dominated
abundance. Other abundant ciliates belonged to
Cyrtophorida,
Peniculida,
Heterotrichida,
Prostomatida,
Hypotrichida,
and
Haptorida.
Shannon-Weaver species diversity had a negative
and significant relationship with chlorophyll a
concentration (r = -0.53, P < 0.05). The ciliate
abundance and biomass, as well as the
environmental variables measured are summarized
in table 1 while table 2 shows the correlations of
environmental variables with ciliate biomass and
with each other. Mean ciliate abundance ranged
from 1.8 ciliates.mL-1 in Lake Malawi to 1,220
ciliates.mL-1 in Lake Elmenteita during the two years
of study. Mean ciliate biomass ranged from 1.9 µg
C.L-1 in Lake Malawi to 1,900 µg C.L-1 in Lake
Sonachi. Ciliate abundance and biomass were
positively related to chlorophyll a concentration
(Figure 2) and to conductivity (Figure 3). Ciliates in
Oligotrichida and Scuticociliatida were the most
abundant in East African lakes. However, the
relative importance of Oligotrichida was greatest in
Lake Malawi (< 5 mg.m-3 chl.), where they
contributed 93.1% of total ciliate abundance and
decreased with increasing chlorophyll, contributing
5.2% in lakes with > 50 mg.m-3 chlorophyll. The
importance of scuticociliates increased with
increasing chlorophyll accounting for 0.7% in Lake
Malawi and 80.2% in lakes with > 50 mg.m-3
chlorophyll (Table 3). The dominance of
Oligotrichida and Scuticociliatida along the
376
conductivity gradient was similar to the trend
observed along the chlorophyll gradient. The mean
size of ciliates ranged from 10.3 ±0.2 µm to 193 ±35
µm (ESD) among lakes. Ciliate biovolume ranged
from 102 to 106 µm3.
Table 3. The contribution to total ciliate abundance
of ciliate orders in East African lakes of different
chlorophyll a concentration.
7
6
contradicts the positive relationship in subtropical
lakes (Beaver & Crisman 1989b), and may be due to
high salinity and probably the large blue-green
algae that dominate saline, eutrophic tropical lakes
and low diversity of edible algae. Beaver & Crisman
(1989) attributed low species diversity of ciliates in
oligotrophic lakes to reduced phytoplankton
abundance and diversity.
Abundance R ? = 0.56
5
Armophorida
Chlorophyll a concentration (mg.m-3)
<5
5 - 50
> 50
0.00
0.03
0.07
Cyrtophorida
0.00
Haptorida
Ciliate orders
4
3
Biomass R ? = 0.33
2
1
0.88
3.36
0.50
3.30
0.99
Hetereotrichida 0.67
3.24
1.30
Hypotrichida
0.00
0.73
1.42
Oligotrichida
93.14
42.61
5.24
Peniculida
0.00
1.96
2.93
Peritrichida
0.00
14.52
1.15
Pleurostomatida 0.00
0.13
1.46
Prostomatida
3.18
1.77
Scuticociliatida 0.67
14.58
80.15
Stichotricha
0.00
1.14
0.01
Suctoria
0.00
0.19
0.12
Tintinnida
0.00
7.07
0.00
Others
4.52
6.46
0.04
0
2
3
4
5
Mean conductivity (uS/cm)
Figure 2. The relationship between mean log10
ciliate abundance and biomass with mean log10
chlorophyll a concentration in East African lakes.
Both abundance and conductivity were log10transformed.
Log10 Ciliate abundance (ciliates.L-1)
Log10 Ciliate biomass (ugC.L-1)
Regression line
y = 0.6454x + 0.0979
4
R? = 0.2385
3
R ? = 0.2637
2
R ? = 0.2385
1
0
0
1
2
3
Log10 Chlorophyll a (mg.m-3)
Figure 3. The relationship between mean ciliate
abundance and biomas with mean conductivity in
East African lakes. Both abundance and conductivity
were log10-transformed.
Discussion
The dominant abundance of Scuticociliates and
Oligotrichs in tropical (East Africa) lakes contrasts to
sub-tropical (Florida) lakes where Oligotrichida,
Scuticociliatida and Haptorida co-dominated (Beaver
& Crisman 1982). Scuticociliates, especially
Cyclidium, were the most abundant ciliates in most
lakes and increased with increasing trophy as in
subtropical and temperate lakes (Beaver & Crisman
1982). The weak negative relationship between
ciliate diversity and trophy in East African lakes
0.50
High salinity reduces the number of species that can
live in lakes (Williams et al. 1990). The ciliate
biovolume ranged from 102 to 106 µm3 but majority
of ciliates were from 103 to 104 µm3, similar to most
ciliates in temperate lakes (Müller 1989). The ciliate
abundance range of 2 to 1,220 ciliates.mL-1 in East
African lakes is larger than reported for temperate of
3.3 cells.mL-1 to 21.6 cells.mL-1 (Pace 1986) and
subtropical lakes of 10.8 to 155.5 ciliates.mL-1
(Beaver & Crisman 1982). Similarly, the biomass
range of 1.9 to 1,900 µg C.L-1 is also higher than
observed in both temperate and subtropical lakes of
12.3 to 56.3 µg C.L-1 (Pace 1986) and 9.3 µg C.L-1
to 126 µg C.L-1 (Beaver & Crisman 1982),
respectively. Both ciliate abundance and biomass
increase with increasing trophy in lakes of the three
zones and from temperate to tropical lakes.
Although not all oligotrophic lakes in East Africa
have higher abundance and biomass than lakes in
the temperate and subtropical zones, tropical lakes
generally have higher ciliate abundance and
biomass, a phenomenon attributed to higher
chlorophyll concentration in tropical lakes. When
regression models predicting abundance and
biomass of ciliates from chlorophyll were compared
for our East African lakes and temperate lakes, the
slopes were not significantly different (ANOVA
interaction, P > 0.05). These results suggest that
temperate, subtropical and tropical lakes have
377
similar ciliate abundance and biomass per unit
chlorophyll. However, some tropical lakes have very
high abundance and biomass of ciliates relative to
chlorophyll probably due to high salinity. Eutrophic,
saline lakes such as Elmenteita, Sonachi and
Bogoria supported a higher abundance of ciliates
probably due to high phytoplankton biomass and
bacterial abundance (> 107 bacteria.ml-1) (e.g.,
Finlay et al. 1987). Since chlorophyll is significantly
higher in East Africa lakes than in subtropical and
temperate lakes (ANOVA, P < 0.05), it appears that
ciliate cell sizes become smaller with increase in
chlorophyll, probably as a response to increasing
availability of bacterial food which also increases
with chlorophyll. Thus, the majority of ciliates in East
African lakes are mainly bacterivorous and
herbivorous. These two trophic groups account for
75% of ciliate population production (Yasindi, 2001).
According to Yasindi (2001) most of this ciliate
production in East African lakes is consumed by
zooplankton, which are, in turn, consumed by fish
(Beadle, 1981; Mwebaza-Ndawula, 1994).
It is clear from this study that both ciliate abundance
and biomass increase with increasing trophy in lakes
of the three zones and from temperate to tropical
lakes. Also East African lakes have higher ciliate
abundance and biomass than subtropical and
temperate lakes mainly due to higher chlorophyll but
the high abundance of bacteria is also important.
Like in temperate and subtropical lakes, herbivorous
ciliates dominate oligotrophic lakes while small
bacterivorous ciliates dominate eutrophic lakes.
Therefore, ciliates form an important linkage through
which production from the microbial loop may be
transferred to the classic food chains in East African
lakes as in temperate waters.
Acknowledgements
This research was supported by a Rockefeller
African Dissertation Internship Award (ADIA) RF
96022 # 785, and a Commonwealth Scholarship (to
A.W.Y.) and the National Science and Engineering
Research Council Grant (to W.D.T.).
References
Beadle, L. C. (1981) The inland waters of tropical Africa. An introduction to tropical limnology. 2nd edition, Longman
London. pp. 475.
Beaver J. R. & Crisman T. L. (1982) The trophic response of ciliated protozoans in freshwater lakes. Limnol. Oceanogr.
22, 246-253.
Beaver J. R. & Crisman T. L. (1989) Analysis of the community structure of planktonic ciliated protozoa relative to trophic
state in Florida lakes. Hydrobiologia 174, 177-184.
Finlay B. J., Curds C. R., Bamforth S. S. & Bafort F. M. (1987) Ciliated protozoa and other microorganisms from two
African lakes, Lake Nakuru and Lake Simbi, Kenya. Arch. Protistenk. 133, 81-91.
Hobbie J. E., Daley R. J. & Jasper S. (1977) Use of nuclepore filters for counting bacteria by fluorescence microscopy.
Applied and Environmental Microbiology, 33, 1225-1228.
Laybourn-Parry J. (1992) Protozoan plankton ecology pp 231. Chapman and Hall, London.
Montagnes D. J. S. & Lynn D. H. (1993) A quantitative protargol stain (QPS) for ciliates and other protists. In: Kemp P.
F., Sherr B. F., Sherr E. B. & Cole J. J. (eds.), Handbook of methods in Aquatic Microbial Ecology pp 229 – 240.
Lewis Publishers, Boca Raton.
Müller H. (1989) The relative importance of different ciliate taxa in the pelagic food web of Lake Constance. Microb. Ecol.
18, 261-273.
Pace M. L. (1986) An empirical analysis of zooplankton community size structure across lake trophic gradients. Limnol.
Oceanogr. 31, 45-55.
Pace M. L. & Orcutt J. D. (1981) The relative importance of protozoans, rotifers, and crustaceans in a freshwater
zooplankton community. Limnol. Oceanogr. 25, 822-830.
Porter K. G., Pace M. L. & Battey J. F. (1979) Ciliate protozoans as links in freshwater planktonic food chains. Nature,
277, 563-565.
Putt M. & Stoecker D. K. (1989) An experimentally determined carbon:volume ratio for marine ‘oligotrichs’ ciliates from
estuarine and coastal waters. Limnol. Oceanogr. 34, 1097-1103.
Statsoft Inc. (1995) Statistica for windows [Computer Program Manual]. Tulsa, OK. Statsoft, Inc., 2325 East 13th Street,
Tulsa, OK, 74104.
Williams W. D., Boulton A. J. & Taaffe R. G. (1990) Salinity as a determinant of salt lake fauna: a question of scale.
Hydrobiologia 197, 257-266.
Yasindi, A. W. (2001) The ecology of planktonic ciliates in tropical lakes of East Africa, Africa. Ph.D Thesis, University of
Waterloo, Waterloo, Ontario, Canada, pp. 221.
Yasindi A. W., Lynn D. H. & Taylor W. D. (2002) Ciliated protozoa in Lake Nakuru, a shallow alkaline-saline lake in
Kenya: seasonal variation, estimated production, and role in the food web. Arch. Hydrobiol. 154, 311–325.
378